An expanded regulatory network temporally controls Candida albicans biofilm formation

Molecular Microbiology

Volumn 96, Issue 6, 2015, Pages 1226-1239

  Fox, Emily P ^a   Bui, Catherine K ^b   Nett, Jeniel E ^c,d   Hartooni, Nairi ^a   Mui, Michael C ^a   Andes, David R ^c,d   Nobile, Clarissa J ^b   Johnson, Alexander D ^a  

^a UNIVERSITY OF CALIFORNIA   (United States)

^b UNIVERSITY OF CALIFORNIA   (United States)

^c UNIVERSITY OF WISCONSIN MADISON   (United States)

^d UNIVERSITY OF WISCONSIN SCHOOL OF MEDICINE AND PUBLIC HEALTH   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

FLO8 PROTEIN; PROTEIN RFX2; REGULATOR PROTEIN; TRANSCRIPTION FACTOR GAL4; UNCLASSIFIED DRUG; FUNGAL PROTEIN;

ADHESION; ARTICLE; BIOFILM; CANDIDA ALBICANS; CHROMATIN IMMUNOPRECIPITATION; DOWN REGULATION; FUNGAL METABOLISM; FUNGUS GROWTH; GENE DELETION; GENE EXPRESSION REGULATION; NONHUMAN; PHENOTYPE; PRIORITY JOURNAL; PROTEIN EXPRESSION; TRANSCRIPTION REGULATION; UPREGULATION; COMPARATIVE STUDY; GENE EXPRESSION; GENETICS; GROWTH, DEVELOPMENT AND AGING; METABOLISM; PHYSIOLOGY;

CANDIDA ALBICANS;

BIOFILMS; CANDIDA ALBICANS; FUNGAL PROTEINS; GENE EXPRESSION;

EID: 84930759319     PISSN: 0950382X     EISSN: 13652958     Source Type: Journal    
DOI: 10.1111/mmi.13002     Document Type: Article

References (57)

1. Andes, D., Nett, J., Oschel, P., Albrecht, R., Marchillo, K., and Pitula, A. (2004) Development and characterization of an in vivo central venous catheter Candida albicans biofilm model. Infect Immun 72: 6023-6031.
2. Argimón, S., Wishart, J.A., Leng, R., Macaskill, S., Mavor, A., Alexandris, T., etal. (2007) Developmental regulation of an adhesin gene during cellular morphogenesis in the fungal pathogen Candida albicans. Eukaryot Cell 6: 682-692.
3. Askew, C., Sellam, A., Epp, E., Hogues, H., Mullick, A., Nantel, A., and Whiteway, M. (2009) Transcriptional regulation of carbohydrate metabolism in the human pathogen Candida albicans. PLoS Pathog 5: e1000612.
4. Baillie, G.S., and Douglas, L.J. (1999) Role of dimorphism in the development of Candida albicans biofilms. J Med Microbiol 48: 671-679.
5. Bonhomme, J., and d'Enfert, C. (2013) Candida albicans biofilms: building a heterogeneous, drug-tolerant environment. Curr Opin Microbiol 16: 398-403.
6. Bonhomme, J., Chauvel, M., Goyard, S., Roux, P., Rossignol, T., and D'Enfert, C. (2011) Contribution of the glycolytic flux and hypoxia adaptation to efficient biofilm formation by Candida albicans. Mol Microbiol 80: 995-1013.
7. Cao, F., Lane, S., Raniga, P.P., Lu, Y., Zhou, Z., Ramon, K., etal. (2006) The Flo8 transcription factor is essential for hyphal development and virulence in Candida albicans. Mol Biol Cell 17: 295-307.
8. Cauda, R. (2009) Candidaemia in patients with an inserted medical device. Drugs 69 (Suppl. 1): 33-38.
9. Chandra, J., Kuhn, D.M., Mukherjee, P.K., Hoyer, L.L., McCormick, T., and Ghannoum, M.A. (2001) Biofilm formation by the fungal pathogen Candida albicans: development, architecture, and drug resistance. J Bacteriol 183: 5385-5394.
10. Chauhan, N.M., Shinde, R.B., and Karuppayil, S.M. (2013) Effect of alcohols on filamentation, growth, viability and biofilm development in Candida albicans. Braz J Microbiol 44: 1315-1320.
11. Desai, J.V., Bruno, V.M., Ganguly, S., Stamper, R.J., Mitchell, K.F., Solis, N., etal. (2013) Regulatory role of glycerol in Candida albicans biofilm formation. MBio 4: 1-9.
12. Du, H., Guan, G., Xie, J., Cottier, F., Sun, Y., Jia, W., etal. (2012) The transcription factor Flo8 mediates CO2 sensing in the human fungal pathogen Candida albicans. Mol Biol Cell 23: 2692-2701.
13. Finkel, J.S., Xu, W., Huang, D., Hill, E.M., Desai, J.V., Woolford, C.A., etal. (2012) Portrait of Candida albicans adherence regulators. PLoS Pathog 8: e1002525.
14. Fox, E.P., and Nobile, C.J. (2012) A sticky situation: untangling the transcriptional network controlling biofilm development in Candida albicans. Transcription 3: 1-8.
15. Fox, E.P., Cowley, E.S., Nobile, C.J., Hartooni, N., Newman, D.K., and Johnson, A.D. (2014) Anaerobic bacteria grow within Candida albicans biofilms and induce biofilm formation in suspension cultures. Curr Biol 24: 2411-2416.
16. García-Sánchez, S., Aubert, S., Iraqui, I., Janbon, G., Ghigo, J., and D'Enfert, C. (2004) Candida albicans biofilms: a developmental state associated with specific and stable gene expression patterns. Eukaryot Cell 3: 536-545.
17. Hao, B., Clancy, C.J., Cheng, S., Raman, S.B., Iczkowski, K.A., and Nguyen, M.H. (2009) Candida albicans RFX2 encodes a DNA binding protein involved in DNA damage responses, morphogenesis, and virulence. Eukaryot Cell 8: 627-639.
18. Hawser, S.P., and Douglas, L.J. (1994) Biofilm formation by Candida species on the surface of catheter materials in vitro. Infect Immun 62: 915-921.
19. Hawser, S.P., Baillie, G.S., and Douglas, L.J. (1998) Production of extracellular matrix by Candida albicans biofilms. J Med Microbiol 47: 253-256.
20. Homann, O.R., Dea, J., Noble, S.M., and Johnson, A.D. (2009) A phenotypic profile of the Candida albicans regulatory network. PLoS Genet 5: e1000783.
21. Inglis, D., Arnaud, M., Binkley, J., Shah, P., Skrzypek, M., Wymore, F., etal. (2012) The Candida genome database incorporates multiple Candida species: multispecies search and analysis tools with curated gene and protein information for Candida albicans and Candida glabrata. Nucleic Acids Res 40: D667-D674.
22. Jabra-Rizk, M.A., Falkler, W.A., and Meiller, T.F. (2004) Fungal biofilms and drug resistance. Emerg Infect Dis 10: 14-19.
23. Kadosh, D., and Johnson, A.D. (2005) Induction of the Candida albicans filamentous growth program by relief of transcriptional repression: a genome-wide analysis. Mol Biol Cell 16: 2903-2912.
24. Kayingo, G., Martins, A., Andrie, R., Neves, L., Lucas, C., and Wong, B. (2009) A permease encoded by STL1 is required for active glycerol uptake by Candida albicans. Microbiology 155: 1547-1557.
25. Kojic, E.M., Darouiche, R.O., and Biofilms, C. (2004) Candida infections of medical devices. Society 17: 255-267.
26. Kunze, D., Melzer, I., Bennett, D., Sanglard, D., MacCallum, D., Nörskau, J., etal. (2005) Functional analysis of the phospholipase C gene CaPLC1 and two unusual phospholipase C genes, CaPLC2 and CaPLC3, of Candida albicans. Microbiology 151: 3381-3394.
27. Liu, H., Köhler, J., and Fink, G.R. (1994) Suppression of hyphal formation in Candida albicans by mutation of a STE12 homolog. Science 266: 1723-1726.
28. López, D., Vlamakis, H., and Kolter, R. (2010) Biofilms. Cold Spring Harb Perspect Biol 2: a000398.
29. Lohse, M.B., and Johnson, A.D. (2010) Temporal anatomy of an epigenetic switch in cell programming: the white-opaque transition of C. albicans. Mol Microbiol 78: 331-343.
30. Martins, M., Henriques, M., Azeredo, J., Rocha, S.M., Coimbra, M.A., and Oliveira, R. (2010) Candida species extracellular alcohols: production and effect in sessile cells. J Basic Microbiol 50: S89-S97.
31. Mukherjee, P.K., Mohamed, S., Chandra, J., Kuhn, D., Liu, S., Antar, O.S., etal. (2006) Alcohol dehydrogenase restricts the ability of the pathogen Candida albicans to form a biofilm on catheter surfaces through an ethanol-based mechanism. Infect Immun 74: 3804-3816.
32. Murillo, L.A., Newport, G., Lan, C., Dungan, J., Agabian, N.M., and Habelitz, S. (2005) Genome-wide transcription profiling of the early phase of biofilm formation by Candida albicans. Eukaryot Cell 4: 1562-1573.
33. Nett, J., Lincoln, L., Marchillo, K., Massey, R., Holoyda, K., Hoff, B., etal. (2007) Putative role of beta-1, 3 glucans in Candida albicans biofilm resistance. Antimicrob Agents Chemother 51: 510-520.
34. Nett, J.E., Lepak, A.J., Marchillo, K., and Andes, D.R. (2009) Time course global gene expression analysis of an in vivo Candida biofilm. J Infect Dis 200: 307-313.
35. Nett, J.E., Sanchez, H., Cain, M.T., and Andes, D.R. (2010a) Genetic basis of Candida biofilm resistance due to drug-sequestering matrix glucan. J Infect Dis 202: 171-175.
36. Nett, J.E., Crawford, K., Marchillo, K., and Andes, D.R. (2010b) Role of Fks1p and matrix glucan in Candida albicans biofilm resistance to an echinocandin, pyrimidine, and polyene. Antimicrob Agents Chemother 54: 3505-3508.
37. Nett, J.E., Marchillo, K., and Andes, D.R. (2012) Host-Fungus Interactions. Totowa, NJ: Humana Press.
38. Nobile, C.J., and Mitchell, A.P. (2005) Regulation of cell-surface genes and biofilm formation by the C. albicans transcription factor Bcr1p. Curr Biol 15: 1150-1155.
39. Nobile, C.J., and Mitchell, A.P. (2007) Microbial biofilms: e pluribus unum. Curr Biol 17: R349-R353.
40. Nobile, C.J., Andes, D.R., Nett, J.E., Smith, F.J., Yue, F., Phan, Q.-T., etal. (2006) Critical role of Bcr1-dependent adhesins in C. albicans biofilm formation in vitro and in vivo. PLoS Pathog 2: e63.
41. Nobile, C.J., Schneider, H.A., Nett, J.E., Sheppard, D.C., Filler, S.G., Andes, D.R., and Mitchell, A.P. (2008) Complementary adhesin function in C. albicans biofilm formation. Curr Biol 18: 1017-1024.
42. Nobile, C.J., Nett, J.E., Hernday, A.D., Homann, O.R., Deneault, J.-S., Nantel, A., etal. (2009) Biofilm matrix regulation by Candida albicans Zap1. PLoS Biol 7: e1000133.
43. Nobile, C.J., Fox, E.P., Nett, J.E., Sorrells, T.R., Mitrovich, Q.M., Hernday, A.D., etal. (2012) A recently evolved transcriptional network controls biofilm development in Candida albicans. Cell 148: 126-138.
44. Noble, S.M., and Johnson, A.D. (2005) Strains and strategies for large-scale gene deletion studies of the diploid human fungal pathogen Candida albicans. Eukaryot Cell 4: 298-309.
45. Noble, S.M., French, S., Kohn, L.A., Chen, V., and Johnson, A.D. (2010) Systematic screens of a Candida albicans homozygous deletion library decouple morphogenetic switching and pathogenicity. Nat Genet 42: 590-598.
46. Raad, I., Hanna, H., and Maki, D. (2007) Intravascular catheter-related infections: advances in diagnosis, prevention, and management. Lancet Infect Dis 7: 645-657.
47. Ramage, G., VandeWalle, K., López-Ribot, J.L., and Wickes, B.L. (2002a) The filamentation pathway controlled by the Efg1 regulator protein is required for normal biofilm formation and development in Candida albicans. FEMS Microbiol Lett 214: 95-100.
48. Ramage, G., Saville, S.P., Wickes, B.L., and López-Ribot, J.L. (2002b) Inhibition of Candida albicans biofilm formation by farnesol, a quorum-sensing molecule. Appl Environ Microbiol 68: 5459-5463.
49. Rane, H.S., Bernardo, S.M., Walraven, C.J., and Lee, S.A. (2012) In vitro analyses of ethanol activity against Candida albicans biofilms. Antimicrob Agents Chemother 56: 4487-4489.
50. Rossignol, T., Ding, C., Guida, A., D'Enfert, C., Higgins, D.G., and Butler, G. (2009) Correlation between biofilm formation and the hypoxic response in Candida parapsilosis. Eukaryot Cell 8: 550-559.
51. Seddiki, S.M.L., Boucherit-Otmani, Z., Boucherit, K., Badsi-Amir, S., Taleb, M., and Kunkel, D. (2013) Assessment of the types of catheter infectivity caused by Candida species and their biofilm formation. First study in an intensive care unit in Algeria. Int J Gen Med 6: 1-7.
52. Sengupta, M., and Datta, A. (2003) Two membrane proteins located in the Nag regulon of Candida albicans confer multidrug resistance. Biochem Biophys Res Commun 301: 1099-1108.
53. Tobudic, S., Kratzer, C., Lassnigg, A., and Presterl, E. (2012) Antifungal susceptibility of Candida albicans in biofilms. Mycoses 55: 199-204.
54. Uppuluri, P., Chaturvedi, A.K., Srinivasan, A., Banerjee, M., Ramasubramaniam, A.K., Köhler, J.R., etal. (2010) Dispersion as an important step in the Candida albicans biofilm developmental cycle. PLoS Pathog 6: e1000828.
55. Wells, M.L., Washington, O.L., Hicks, S.N., Nobile, C.J., Hartooni, N., Wilson, G.M., etal. (2015) Post-transcriptional regulation of transcript abundance by a conserved member of the tristetraprolin family in Candida albicans. Mol Microbiol 95: 1036-1053.
56. Yeater, K.M., Chandra, J., Cheng, G., Mukherjee, P.K., Zhao, X., Rodriguez-Zas, S.L., etal. (2007) Temporal analysis of Candida albicans gene expression during biofilm development. Microbiology 153: 2373-2385.
57. Zarnowski, R., Westler, W.M., Lacmbouh, G.A., Marita, J.M., Bothe, J.R., Bernhardt, J., etal. (2014) Novel entries in a fungal biofilm matrix encyclopedia. MBio 5: e01333-14.